Integrated elemental analysis supports targeting copper perturbations as a therapeutic strategy in multiple sclerosis

Neurotherapeutics. 2024 Sep;21(5):e00432. doi: 10.1016/j.neurot.2024.e00432. Epub 2024 Aug 19.

Abstract

Multiple sclerosis (MS) is a debilitating affliction of the central nervous system (CNS) that involves demyelination of neuronal axons and neurodegeneration resulting in disability that becomes more pronounced in progressive forms of the disease. The involvement of neurodegeneration in MS underscores the need for effective neuroprotective approaches necessitating identification of new therapeutic targets. Herein, we applied an integrated elemental analysis workflow to human MS-affected spinal cord tissue utilising multiple inductively coupled plasma-mass spectrometry methodologies. These analyses revealed shifts in atomic copper as a notable aspect of disease. Complementary gene expression and biochemical analyses demonstrated that changes in copper levels coincided with altered expression of copper handling genes and downstream functionality of cuproenzymes. Copper-related problems observed in the human MS spinal cord were largely reproduced in the experimental autoimmune encephalomyelitis (EAE) mouse model during the acute phase of disease characterised by axonal demyelination, lesion formation, and motor neuron loss. Treatment of EAE mice with the CNS-permeant copper modulating compound CuII(atsm) resulted in recovery of cuproenzyme function, improved myelination and lesion volume, and neuroprotection. These findings support targeting copper perturbations as a therapeutic strategy for MS with CuII(atsm) showing initial promise.

Keywords: Copper; CuATSM; Multiple sclerosis (MS); Neurodegeneration; Neuroprotection; Therapeutics.

MeSH terms

  • Animals
  • Coordination Complexes
  • Copper* / metabolism
  • Encephalomyelitis, Autoimmune, Experimental* / drug therapy
  • Encephalomyelitis, Autoimmune, Experimental* / metabolism
  • Female
  • Humans
  • Mice
  • Mice, Inbred C57BL
  • Multiple Sclerosis* / drug therapy
  • Multiple Sclerosis* / metabolism
  • Organometallic Compounds
  • Spinal Cord* / drug effects
  • Spinal Cord* / metabolism
  • Spinal Cord* / pathology
  • Thiosemicarbazones

Substances

  • Copper
  • Organometallic Compounds
  • copper (II) diacetyl-di(N(4)-methylthiosemicarbazone)
  • Coordination Complexes
  • Thiosemicarbazones